Tracing the Evolutionary Origin of the Gut–Brain Axis

Abstract

Colonization of body epithelial surfaces with a rather specific microbial community is a fundamental feature of all animals. Recent studies suggest that in mammals the enteric microbiota has a bidirectional communication with the nervous system. The complexity of these interactions is referred to as “gut–brain axis”. Highlighting the significance of these interactions are studies in mice which show that the intestinal microbiota can directly affect complex behaviour. The origin and ancestral function of these interactions are not well understood. Here, I review findings that neurons in the early emerging metazoan Hydra secrete neuropeptides which shape the microbiome on the body surface. I also discuss recent observations which indicate that symbiotic bacteria modulate spontaneous body contractions in Hydra. Germ-free polyps show strongly reduced and less regular spontaneous contraction frequencies. The effects on contraction frequency were partially restored by reconstituting the natural microbiota. These findings strongly suggest that the influence of bacteria on neuronal activity is the outcome of an evolutionary ancient interaction between bacteria and metazoans, opening a window into investigating the basic mechanisms of, for example, neurological disorders in vertebrates.

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Acknowledgements

I am particularly thankful to René Augustin, Sebastian Fraune, Alexander Klimovich, and Andrea Murillo-Rincon for their pioneering contributions towards uncovering microbe–neuron interactions in Hydra. I thank Andrea Murillo-Rincon and Alexander Klimovich for providing pictures and figures for this review. And I gratefully appreciate the support from the Canadian Institute for Advanced Research (CIFAR). This work was supported by the Deutsche Forschungsgemeinschaft (DFG) (CRC1182 “Origin and Function of Metaorganisms”, DFG grant BO 848/15-3, and grants from the DFG Cluster of Excellence programme “Inflammation at Interfaces”).